During this time, Crayston also became an England international; he made his debut in a 3-1 win against Germany on December 41935, and in all won eight caps for his country between 1935 and 1937, scoring one goal. His final cap came in a 5-4 win against Czechoslovakia on December 11937.

Like many of his contemporaries, the Second World War robbed Crayston of what should have been the peak of his career; he joined the Royal Air Force whilst still playing irregular wartime football. However, a serious knee injury in a wartime match against West Ham United in 1943 forced Crayston to retire from playing. He played 207 matches in total (168 league matches), scoring 17 goals (16 league goals).

After his premature retirement and demobbing from the RAF, Crayston moved into coaching, and in June 1947 he became assistant to new Arsenal manager Tom Whittaker. After Whittaker's death in 1956, Crayston became caretaker manager on October 241956 and permanent manager on December 211956. However, his stewardship of the team was brief and unsuccessful; unable to bring any new players in, the team started to decline. In 1957-58 Arsenal slipped to 12th in the League (their worst position for 38 years) and faced a humiliating FA Cup defeat at the hands of Third Division SouthNorthampton Town. Disillusioned, in May 1958 he resigned as Arsenal manager, and took up the reins at Doncaster Rovers a couple of months later, holding the post until his retirement from the game in 1961. He died in 1992, at the age of 82.